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Influence of dietary cobalt source and concentration on performance, vitamin B₁₂ status, and ruminal and plasma metabolites in growing and finishing steers^1,2

M. E. Tiffany^*, J. W. Spears^*,3, L. Xi^* and J. Horton^,4

^* Department of Animal Science, North Carolina State University, Raleigh 27695-7621 and and Kemin Americas, Des Moines, IA 50301-0070

	Abstract

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Sixty Angus steers, averaging 274 kg, were used to evaluate the effects of Co source and concentration on performance, vitamin B₁₂ status, and metabolic characteristics of steers. Treatments consisted of 0 (control, analyzed 0.04 mg Co/kg), 0.05, 0.10, and 1.0 mg of supplemental Co/kg of DM from CoCO₃ or 0.05 and 0.10 mg of supplemental Co/kg of DM from Co propionate. Steers were individually fed a growing diet for 56 d followed by a high-concentrate finishing diet. Performance was not affected by Co supplementation during the growing phase. During the finishing phase, ADFI (DM basis) and ADG were higher (P < 0.05) for the entire finishing phase, and gain:feed was higher (P < 0.10) over the first 56 d for Co-supplemented steers. Steers supplemented with 0.10 mg Co/kg as Co propionate had higher (P < 0.05) ruminal propionate and lower (P < 0.05) acetate molar proportions than steers receiving 0.10 Co/kg as CoCO₃ during the growing phase. Supplemental Co increased (P < 0.10) molar proportion of propionate during the finishing phase. Plasma vitamin B₁₂ was higher (P < 0.05) in Co-supplemented steers by d 56 of the growing phase and remained higher (P < 0.10) throughout the study. Control steers had higher (P < 0.05) plasma methylmalonic acid on d 56 of the growing phase and on d 28, 56, and 112 of the finishing phase than steers receiving supplemental Co. Steers supplemented with Co had higher plasma glucose at d 56 (P < 0.01), 84 (P < 0.10), and 112 (P < 0.01) of the finishing phase. Steers supplemented with 0.10 mg Co/kg as Co propionate had higher plasma glucose than those receiving 0.10 mg Co/kg as CoCO₃ at d 28 of the growing phase (P < 0.05) and d 28 of the finishing phase (P < 0.10). Final body weight and hot carcass weight were lower (P < 0.10) in steers receiving the control diet, whereas other carcass characteristics were not affected by dietary Co. Average daily gain and feed efficiency for the entire finishing phase did not differ among Co-supplemented steers. However, increasing supplemental Co above 0.05 mg/kg DM (total diet Co = 0.09 mg/kg) resulted in increased (P < 0.01) plasma (linear) and liver (quadratic) vitamin B₁₂ concentrations and decreased (quadratic, P < 0.10) plasma methylmalonic acid concentrations toward the end of the finishing phase. These results suggest that finishing steers require approximately 0.15 mg Co/kg of DM. Vitamin B₁₂ status was not affected by Co source; however, the two Co sources seemed to affect certain metabolites differently.

Key Words: Cattle • Cobalt • Vitamin B₁₂

	Introduction

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Dietary Co is required by ruminal microorganisms for its addition to the corrin ring structure during the complex formation of vitamin B₁₂. Ruminant diets deficient in Co result in decreased microbial vitamin B₁₂ biosynthesis in the rumen, limiting the amount of vitamin B₁₂ available to microbes and the host animal. In higher animals, vitamin B₁₂ is a cofactor for two enzymes, methylmalonyl-CoA mutase and methionine synthase. The former catalyzes the interconversion of methylmalonyl-CoA to succinyl-CoA (Banerjee and Chowdhury, 1999), an important step in glucogenesis, whereas the latter acts to remethylate homocysteine, in the terminal step of methionine synthesis (Matthews, 1999). In ruminants, a Co-induced vitamin B₁₂ deficiency results in reduced intake and ADG, decreased plasma and liver vitamin B₁₂, elevated plasma methylmalonic acid (MMA) and homocysteine (Stangl et al., 1999, 2000), and decreased methionine synthase and methylmalonyl-CoA mutase activities in tissues (Kennedy et al., 1990).

Cobalt requirements of growing and finishing cattle are poorly defined, and the current NRC (1996) recommendation of 0.10 mg Co/kg DM is based on older data obtained primarily from grazing studies (Smith, 1987). Recent studies (Schwarz et al., 2000; Stangl et al., 2000) suggest that growing German Simmental bulls, fed a corn silage-based diet, require approximately 0.20 mg Co/kg DM. Limited research has evaluated the bioavailability of various supplemental Co sources (Kawashima et al., 1997a,b), and no research has compared bioavailability of different Co sources when supplemented to ruminant diets at physiological concentrations. Our hypothesis was that the NRC recommendation of 0.10 mg Co/kg DM is below the Co requirement of growing and finishing cattle. The present study was conducted to estimate Co requirements of growing and finishing steers and to compare the relative bioavailability of Co from CoCO₃ and Co propionate.

	Materials and Methods

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General

Sixty Angus steers (274.2 kg initial BW) were used in this experiment. Care, handling, and sampling of the animals herein were approved by the North Carolina State University Animal Care and Use Committee. Steers were obtained from the Upper Piedmont Research Station, at Reidsville, NC, or were purchased at feeder calf sales in North Carolina. After arrival, steers were ear-tagged, weighed, vaccinated with Bovashield 4 (Pfizer Animal Health, Exton, PA) and Vision 7 (Bayer Corp., Shawnee Mission, KS), wormed with Safe Guard (Hoechst Roussel Vet., Clinton, NJ), and confined to fescue pasture for 53 d where they were supplemented with corn silage (2.0 kg DM•hd^-1•d^-1). Steers were then weighed on two consecutive days and allotted by weight and origin to one of five, 12-animal pens equipped with individual Calan gate feeders (American Calan, Northwood, NH). Steers were housed in covered, slotted-floor pens (5 m x 10 m) for the duration of the experiment.

Growing Phase

After adjusting to the Calan gate feeding system, steers were weighed on two consecutive days, implanted with Synovex-S (Fort Dodge Animal Health, Fort Dodge IA), bled via jugular venipuncture, biopsied for a liver sample, and assigned randomly within a pen (two steers per treatment per pen) to one of six treatments. Treatments consisted of 1) control (no supplemental Co), 2) 0.05 mg of supplemental Co/kg DM from Co carbonate (CoCO₃), 3) 0.10 mg of supplemental Co/kg DM from CoCO₃, 4) 1.00 mg of supplemental Co/kg DM from CoCO₃, 5) 0.05 mg of supplemental Co/kg DM from Co propionate (CoPr; Kemin Americas, Des Moines, IA), and 6) 0.10 mg of supplemental Co/kg DM from CoPr.

During the 56-d growing phase, steers were fed a corn-cottonseed hull-soybean meal based diet (Table 1; basal diet contained 0.04 mg Co/kg of DM). The diet was formulated to meet or exceed nutrient requirements for growing beef steers with the exception of Co (NRC, 1996). Diets were fed once daily in amounts sufficient to provide ad libitum access to feed. Feed offerings were recorded on a daily basis and refusals recorded every 14 d. On days when blood and ruminal fluid samples were collected, feeding times were staggered to allow samples to be obtained 2 h after feeding.

On d 56, ruminal fluid was collected by stomach tube. Ruminal fluid was strained through four layers of cheesecloth, and 10 mL was added to a vial containing 2 mL of meta-phosphoric acid (25% wt/vol). The sample was placed on ice and transported to the laboratory where it was frozen at -70°C until analysis for VFA.

Liver biopsies were obtained initially and on d 56, through an incision made between the 11th and 12th rib on a line from the tuber coxae to the point of the shoulder. Before incision, biopsy sites were clipped of hair, scrubbed with Betadine (Purdue Fredrick, Norwalk, CT), and subsequently scrubbed with 70% (vol/vol) ethyl alcohol. A core sample of liver was obtained using a modified Jan Shide bone marrow biopsy punch (0.4 cm diameter x 10 cm in length), via the true-cut technique (Pearson and Craig, 1980). Liver samples were rinsed without delay using 0.10 M physiological buffered saline solution (pH 7.4) and drained to remove blood. The samples were placed in acid-washed polyethylene tubes, capped, placed on dry ice, and subsequently transported to the laboratory where they were frozen at -70°C.

Finishing Phase

During the finishing phase, steers received the same dietary treatments as defined in the growing phase, but were switched to a high-concentrate diet (Table 1) over a 7-d period (basal diet contained 0.04 mg Co/kg of DM). Feed offered and refused were measured and recorded as previously described for the growing phase.

Steers were implanted with Synovex-Plus (Fort Dodge Animal Health) at the beginning of the finishing phase. Steers were weighed and blood samples collected at 28-d intervals through d 112 of the finishing phase. A liver biopsy sample was collected on d 56 in the manner previously described. Equal numbers of steers per treatment were slaughtered after receiving the finishing diet for either 112 d (three heaviest pens, n = 36) or 127 d (two lightest pens, n = 24). Final weights were recorded on two consecutive days, and steers were slaughtered at a commercial abattoir following an overnight fast. Final liver samples were collected postmortem and immediately placed on dry ice for transport to the laboratory, where they were frozen at -70°C.

Analytical Procedures

Feed samples for the analysis of Co where prepared using a microwave digestion (Mars 5, CEM Corp., Matthews, NC) procedure described by Gengelbach et al. (1994). Cobalt was determined by flameless atomic absorption spectrophotometry using a graphite furnace (GFA-6500, Shimadzu Scientific Instruments, Kyoto, Japan).

Plasma and liver vitamin B₁₂ concentrations were determined using a competitive binding radioimmunoassay kit (ICN, Costa Mesa, CA), in which nonspecific vitamin B₁₂ binding R-proteins were removed by affinity chromatography. Prior to liver vitamin B₁₂ quantification, a tissue homogenate was prepared using a borate buffer (pH 9.2, Fisher Scientific, Suwanee GA) and 1% bovine serum albumin (Sigma-Aldrich, St. Louis, MO) as described by Stangl et al. (1999).

Plasma samples for the determination of MMA were prepared according to the method of McMurray et al. (1986) using a modified GC method. The GC (Hewlett-Packard Model 5890 Series II, Palo Alto, CA) was equipped with a 25 m x 0.32 mm x 0.17µm methyl siloxane column (Agilent Technologies, Wilmington, DE), on which 1.0 µL of acetyl chloride-butan-1-ol derivatized sample was injected. The oven temperature program utilized was 100°C initial followed by a ramp of 10°C/min to 155°C for 2 min, followed by a ramp of 10°C/min to 215°C, where the temperature was held for 10 min to flush the column. Plasma glucose was determined by a membrane-immobilized glucose oxidase enzyme coupled to an electrochemical sensor (Model 27 Industrial Analyzer; Yellow Springs Instrument Co., Inc., Yellow Springs, OH).

Ruminal fluid VFA concentrations were determined by GC (Varian Instruments Model 3800, Walnut Creek, CA) using a Nikol fused-silica column, 15 m x 0.53 mm x 0.50 µm (Supelco, Bellefonte, PA). The oven temperature program began with an initial temperature of 80°C, followed by a ramp of 20°C/min to 140°C, which was held for 2 min. Temperature was then ramped 30°C/min to 175°C, where it was held for 1 min to flush the column.

Data were analyzed as a randomized complete block design using the GLM procedure of SAS (SAS Inst. Inc., Cary, NC). The model for performance variables, ruminal VFA, and carcass data contained treatment and pen. Liver vitamin B₁₂ and plasma variables were analyzed as repeated measures with animal within treatment as the error term for treatment effects. When a treatment x time interaction was observed, data were analyzed by sampling day and initial values were used as a covariant when appropriate. Planned orthogonal contrasts were used to detect differences among means. The comparisons made were 1) control vs. all Co-supplemented treatments, 2) 0.05 mg Co/kg DM from CoCO₃ vs. 0.05 mg Co/kg DM from CoPr, 3) 0.10 mg Co/kg DM from CoCO₃ vs. 0.10 mg Co/kg DM from CoPr, 4) linear, and 5) quadratic effects of Co level (CoCO₃ treatments only). Because the supplemental Co levels were unequally spaced (0, 0.05, 0.10, 1.0, for CoCO₃), coefficients used to construct polynomials for linear and quadratic contrasts were calculated as described by Robson (1959).

	Results and Discussion

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Performance

Steer performance during the 56-d growing phase was not affected by Co source or concentration (Table 2). Cobalt addition to the control diet increased ADG (P < 0.05) during the first 56 d of the finishing phase (Table 2). Gain by control steers did not differ from Co-supplemented steers between d 56 and 112 of the finishing period; however, steers supplemented with 0.05 mg Co/kg DM, from CoCO₃, tended to gain faster than the other treatment groups during this period. The contrast comparing 0.05 mg Co/kg DM from CoCO₃ and CoPr was significant (P < 0.05). It is unclear why gains were greater in steers supplemented with 0.05 mg Co/kg DM from d 56 to 112. Average daily gain for the entire finishing phase was increased (P < 0.05) by Co supplementation but was not affected by Co source.

A major physiologic effect of cobalt–vitamin B₁₂ deficiency is loss of appetite (Smith, 1997). Early attempts to define Co requirements (Marston, 1970) and experiments that showed the detrimental effects of Co-vitamin B₁₂ deficiency on intakes and live weights, used hay-fed sheep (Smith and Marston, 1970). More recently, Schwarz et al. (2000) conducted an experiment to determine the Co requirements of growing Simmental beef bulls consuming a corn silage-rich diet (basal diet 0.07 mg Co/kg diet) fortified with graduated concentrations of CoSO₄. Intake of the unsupplemented control group changed little over the 266-d period, but intake was lower than for those supplemented with Co. As a result of their work, they suggested that 0.16 to 0.18 mg of dietary Co/kg is necessary to maximize intake. In the present study, intake was not affected by supplemental Co during the 56-d growing phase. Although lesser than Co-supplemented groups, intake by control steers increased during the finishing phase, even though the control diet had less Co than the diet described by Schwarz et al. (2000). The degree to which storage of vitamin B₁₂ in tissues and differences in diet composition contribute to the initial onset of decreased intake is uncertain. For the total finishing phase, intake increased quadratically (P < 0.05) in the present study, with feed intake highest in steers supplemented with 1.0 mg Co/kg DM. This suggests that dietary Co concentrations above the 0.10 mg/kg of DM level recommended by NRC (1996) may increase intake. These data agree with the results of Schwarz et al. (2000).

Work by Schwarz et al. (2000) determined that diets containing 0.07 mg Co/kg resulted in lower daily gains in German Simmental bulls than those containing at least 0.11 mg Co/kg. Their analysis of data, using a broken-line model, suggested that the optimum concentration of dietary Co for gain was 0.12 mg/kg DM. In the present study, steers fed the control diet containing 0.04 mg Co/kg DM, had lesser gains than Co-supplemented steers during the finishing phase. The increase in gain:feed for Co-supplemented steers over the first 56 d of the finishing period diminished during the second 56-d period so that total gain:feed was not affected by Co supplementation. Performance data suggest that the control diet was only marginally deficient in Co and that the response to Co supplementation was greater early in the finishing phase. Despite the higher feed intake observed in steers supplemented with 1.0 mg Co/kg DM, the addition of 0.05 mg Co/kg DM (total dietary Co of 0.09 mg Co/kg of DM) seemed to be sufficient for maximal gain and feed efficiency.

Vitamin B₁₂ Status

Plasma vitamin B₁₂ was affected by a treatment x time (P < 0.01) interaction (Table 3). By d 56 of the growing phase and at all sampling days during the finishing phase steers receiving supplemental Co had higher (P < 0.05) plasma vitamin B₁₂ concentrations than controls. Increasing dietary Co (from CoCO₃) resulted in a quadratic increase (P < 0.05) in plasma vitamin B₁₂ concentrations on d 56 of the growing phase and on d 28 and 56 of the finishing phase. Plasma vitamin B₁₂ responded in a linear (P < 0.01) manner to increasing dietary Co on d 84 and 112 of the finishing phase. In general, increasing supplemental Co from 0.05 to 0.10 mg/kg DM resulted in small changes in plasma vitamin B₁₂; however, plasma vitamin B₁₂ concentrations were greatly increased when supplemental Co was increased from 0.10 to 1.0 mg/kg DM. This suggests that addition of 1.0 mg Co/kg diet DM greatly increased synthesis of vitamin B₁₂ by ruminal microorganisms, compared to the low Co additions. Vitamin B₁₂ concentration in plasma was unaffected by cobalt source during the growing or finishing phase.

Numerous studies in sheep (Kercher and Smith, 1956; Somers and Gawthorne, 1969; Marston, 1970) have shown that Co supplementation to Co-deficient diets greatly increases vitamin B₁₂ concentrations in plasma and liver. However, relatively few studies have investigated the effects of dietary Co on blood and liver vitamin B₁₂ concentrations of cattle, particularly those fed high-energy diets. In agreement with the present study, Co supplementation to corn silage-based diets, containing 0.07 to 0.08 mg Co/kg DM, increased plasma and liver vitamin B₁₂ concentrations in growing German Simmental males (Stangl et al., 1999; 2000). Based on samples obtained at the end of a 40-wk study, Stangl et al. (2000) concluded that a dietary concentration of 0.25 mg Co/kg DM was required for maximum plasma and liver vitamin B₁₂ concentrations. Plasma vitamin B₁₂ concentrations increased greatly, whereas liver vitamin B₁₂ increased slightly in the present study when supplemental Co was increased from 0.1 to 1.0 mg/kg DM. Because no dietary Co concentrations were evaluated between 0.1 and 1.0 mg/kg DM, results obtained from the present study do not allow for estimation of minimal Co requirement for maximal plasma or liver vitamin B₁₂ concentrations. In humans, biliary excretion of vitamin B₁₂ is substantial (Castle and Hale, 1998), but little is known about vitamin B₁₂ excretion in ruminants. In lactating dairy cows fed diets high in Co, urinary vitamin B₁₂ concentrations were greater than vitamin B₁₂ concentrations in serum or milk (Walker and Elliot, 1972). Because liver vitamin B₁₂ concentrations in the present study reflected a minimal increase relative to plasma increases in steers supplemented with 1.0 mg Co/kg DM, it is likely that the excess vitamin B₁₂ was excreted in bile and urine.

Plasma Methylmalonic Acid and Glucose

Plasma MMA was affected by time (P < 0.01) and tended (P = 0.11) to be affected by a treatment x time interaction (Table 4). Plasma MMA was not affected by Co source during the growing or finishing phase. Plasma MMA decreased in a quadratic manner on d 56 (P < 0.01) of the growing phase and d 28 (P < 0.01), 56 (P < 0.10), and 112 (P < 0.10) of the finishing phase in response to increasing dietary concentrations of Co. Because MMA is the substrate for the vitamin B₁₂-dependent enzyme, methylmalonyl-CoA mutase, the greater plasma concentrations of MMA in steers fed the low-Co diet likely reflect reduced activity of this enzyme. Kennedy et al. (1991) described the steady increase of plasma MMA, as plasma vitamin B₁₂ concentrations decreased in lambs fed a barley diet low (0.04 mg/kg) in Co. High-grain diets have been associated with increased urinary MMA in sheep (Lough and Calder, 1976). This could be the result of increased propionate molar proportions, when high-grain diets are fed, increasing the demand on methylmalonyl-CoA mutase in propionate metabolism. This may explain the greater MMA concentrations observed in steers of all treatment groups, during the finishing phase. Studies using cattle have also been conducted to evaluate the effectiveness of using MMA as a diagnostic tool for Co deficiency (Paterson and MacPherson, 1990), and to define Co requirements based on plasma MMA and other metabolites (Stangl et al., 2000). Stangl et al. (2000) reported a linear decrease in plasma MMA when dietary Co was increased from 0.07 to 0.147 mg/kg of DM. Increasing dietary Co above 0.147 mg/kg of DM resulted in little or no change in plasma MMA concentrations. In agreement with these findings, plasma MMA concentrations on several sampling days in the present study tended to be slightly lower in steers receiving total dietary Co concentrations of 0.14 mg/kg (0.10 mg/kg supplemental) compared with those fed 0.09 mg Co/kg of DM (0.05 mg/kg supplemental).

Molar proportions of VFA were not affected by the addition of supplemental Co to the basal diet during the growing phase (Table 6). However, the contrast comparing the two sources supplemented at 0.10 mg Co/kg DM differed (P < 0.05) for acetate, propionate, butyrate, and acetate:propionate ratio. Steers receiving supplemental Co as CoPr had greater molar proportions of propionate (P < 0.05) and lesser molar proportions of acetate (P < 0.05) and butyrate (P < 0.05). The increased propionate and decreased acetate resulted in a decreased (P < 0.05) acetate:propionate ratio. The CoPr treatment (0.10 mg Co/kg) only supplied 0.27 mg propionate/kg of DM. Therefore, the greater molar proportion of propionate observed in steers supplemented with 0.10 mg Co/kg DM, from CoPr, cannot be explained by propionate derived from dietary addition of CoPr.

Carcass Characteristics

Steers receiving supplemental Co had higher (P < 0.10) hot carcass weights than controls (Table 7). Dressing percent and longissimus muscle area were not affected by Co source or concentration. As supplemental Co increased, there was a quadratic effect (P < 0.10) on marbling scores. Supplemental Co did not affect backfat or kidney, pelvic, and heart fat; however, steers receiving supplemental Co as CoPr at 0.05 mg Co/kg had slightly lower backfat (P < 0.05) and yield grade (P < 0.10) than those supplemented with CoCO₃. Dietary Co affected quality grades in a quadratic (P < 0.05) manner, with quality grades being lower in steers supplemented with 1.0 mg Co/kg DM. Few studies have reported the effects of dietary Co on carcass characteristics. Schwarz et al. (2000) found that Simmental bulls fed a diet containing 0.07 mg Co/kg DM had lighter carcass weights and less renal fat than those receiving diets containing at least 0.11 mg Co/kg DM.

In conclusion, the present study indicates that increasing dietary Co above the current NRC requirement of 0.10 mg/kg DM will greatly increase plasma and moderately increase liver vitamin B₁₂ concentrations in finishing steers. Based on performance and vitamin B₁₂ status, the control diet containing 0.04 mg Co/kg DM was clearly inadequate in Co. At a number of sampling dates, steers supplemented with 0.10 mg Co/kg DM or higher had lower plasma MMA concentrations than steers supplemented with 0.05 mg Co/kg DM. Although 0.05 mg supplemental Co/kg DM (total diet Co of 0.09 mg/kg) seemed to maximize gain and feed efficiency, the slightly greater plasma MMA concentrations in steers supplemented with 0.05 mg Co/kg suggest that with this level of Co, vitamin B₁₂ limited conversion of methylmalonyl-CoA to succinyl CoA. Plasma MMA concentrations were generally similar in steers supplemented with 0.10 or 1.00 mg Co/kg. Plasma vitamin B₁₂ concentrations were greater in steers supplemented with 1.00 mg Co/kg compared to those receiving 0.10 mg Co/kg DM during the finishing phase. However, the concentration of plasma vitamin B₁₂ observed in steers supplemented with 1.00 mg Co/kg DM likely exceeded the mammalian vitamin B₁₂ requirement because liver vitamin B₁₂ and plasma MMA concentrations changed only slightly when supplemental Co was increased from 0.10 to 1.00 mg/kg DM. Collectively, these data suggest that the dietary Co (diet plus supplemental) requirement of growing and finishing steers is approximately 0.15 mg/kg diet DM.

	Implications

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Results of the present study indicate that the current NRC requirement for cobalt of 0.10 mg/kg of the diet is probably marginal for growing and finishing steers. Increasing total dietary cobalt above 0.09 mg/kg of the diet increased vitamin B₁₂ status and decreased plasma concentrations of methylmalonic acid. Based on results of the current study, a cobalt requirement of 0.15 mg/kg of diet is recommended. Cobalt carbonate and cobalt propionate were used with similar efficiency by ruminal microorganisms for vitamin B₁₂ synthesis; however, the two cobalt sources seemed to affect certain metabolic variables differently.

	Footnotes

 
¹ Use of trade names in this publication does not imply endorsement by the North Carolina Agric. Res. Serv. or criticism of similar products not mentioned.

² This research was supported in part by a gift from Kemin Americas, Des Moines, IA.

⁴ Present address: Nutrition Service Associates, P.O. Box 350, Hereford, TX 79045.

³ Correspondence—phone: 919/515-4008; fax: 919/515-4463; E-mail: Jerry_Spears{at}ncsu.edu.

Received for publication April 8, 2003. Accepted for publication August 21, 2003.

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